Locus-specific paramutation in Zea mays is manifest by a chromodomain helicase DNA-binding 3 nucleosome remodeler controlling development and pollen function

Paramutations represent directed and meiotically-heritable changes in gene regulation leading to apparent violations of Mendelian inheritance. Although the mechanism and evolutionary importance of paramutation behaviors remains largely unknown, genetic screens in maize (Zea mays) have identified five components affecting 24 nucleotide RNA biogenesis as being required to maintain transcriptional or post-transcriptional repression of a paramutant purple plant1 allele. RNA polymerase IV’s largest subunit represents the only described component that also specifies tissue-specific expression patterns for certain alleles. Here we show that two genetic screens identify a chromodomain helicase DNA-binding 3 protein orthologous to Arabidopsis (Arabidopsis thaliana) PICKLE as a second component controlling somatic development. Genetic and in vitro tests show this protein also contributes to male gametophyte function. Cross-species comparisons of the corresponding Arabidopsis and maize mutants highlight a conserved developmental program with genes responsible for gibberellin biosynthesis as common dysregulated targets. In contrast, developmental pathways affected by the two paramutation mutants are largely distinct, yet both repress RNA levels from a putative FACTOR OF DNA METHYLATION 1 ortholog. Our results indicate that nucleosome positioning, influenced by both mitotically and meiotically-heritable feature(s), is responsible for manifesting both paramutations and normal plant ontogeny.